Metabolomic profiling of wild-type and mutant soybean root nodules using laser-ablation electrospray ionization mass spectrometry reveals altered metabolism.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
08 2020
Historique:
received: 19 06 2019
revised: 05 04 2020
accepted: 17 04 2020
pubmed: 16 5 2020
medline: 13 4 2021
entrez: 16 5 2020
Statut: ppublish

Résumé

The establishment of the nitrogen-fixing symbiosis between soybean and Bradyrhizobium japonicum is a complex process. To document the changes in plant metabolism as a result of symbiosis, we utilized laser ablation electrospray ionization-mass spectrometry (LAESI-MS) for in situ metabolic profiling of wild-type nodules, nodules infected with a B. japonicum nifH mutant unable to fix nitrogen, nodules doubly infected by both strains, and nodules formed on plants mutated in the stearoyl-acyl carrier protein desaturase (sacpd-c) gene, which were previously shown to have an altered nodule ultrastructure. The results showed that the relative abundance of fatty acids, purines, and lipids was significantly changed in response to the symbiosis. The nifH mutant nodules had elevated levels of jasmonic acid, correlating with signs of nitrogen deprivation. Nodules resulting from the mixed inoculant displayed similar, overlapping metabolic distributions within the sectors of effective (fix

Identifiants

pubmed: 32410239
doi: 10.1111/tpj.14815
doi:

Substances chimiques

Carbon 7440-44-0
Nitrogen N762921K75

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1937-1958

Informations de copyright

© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Atkins, C. (1987) Metabolism and translocation of fixed nitrogen in the nodulated legume. Plant Soil, 100, 157-169.
Babu-Khan, S., Yeo, T.C., Martin, W.L., Duron, M.R., Rogers, R.D. and Goldstein, A.H. (1995) Cloning of a mineral phosphate-solubilizing gene from Pseudomonas cepacia. Appl. Environ. Microbiol. 61, 972-978.
Banba, M., Siddique, A.-B.-M., Kouchi, H., Izui, K. and Hata, S. (2001) Lotus japonicus forms early senescent root nodules with Rhizobium etli. Mol. Plant-Microbe Interact. 14, 173-180.
Baral, B., da Silva, J.A.T. and Izaguirre-Mayoral, M.L. (2016) Early signaling, synthesis, transport and metabolism of ureides. J. Plant Physiol. 193, 97-109.
Barsch, A., Carvalho, H.G., Cullimore, J.V. and Niehaus, K. (2006a) GC-MS based metabolite profiling implies three interdependent ways of ammonium assimilation in Medicago truncatula root nodules. J. Biotechnol. 127, 79-83.
Barsch, A., Tellström, V., Patschkowski, T., Küster, H. and Niehaus, K. (2006b) Metabolite profiles of nodulated alfalfa plants indicate that distinct stages of nodule organogenesis are accompanied by global physiological adaptations. Mol. Plant-Microbe Interact. 19, 998-1013.
Beach, D.G., Walsh, C.M., Cantrell, P., Rourke, W., O'Brien, S., Reeves, K. and McCarron, P. (2016) Laser ablation electrospray ionization high-resolution mass spectrometry for regulatory screening of domoic acid in shellfish. Rapid Commun. Mass Spectrom. 30, 2379-2387.
Beatty, P.H. and Good, A.G. (2011) Future prospects for cereals that fix nitrogen. Science, 333, 416-417.
Bolon, Y.T., Haun, W.J., Xu, W.W. et al. (2011) Phenotypic and genomic analyses of a fast neutron mutant population resource in soybean. Plant Physiol. 156, 240-253.
Brechenmacher, L., Lei, Z., Libault, M., Findley, S., Sugawara, M., Sadowsky, M.J., Sumner, L.W. and Stacey, G. (2010) Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum. Plant Physiol. 153, 1808-1822.
Brewin, N.J. (1991) Development of the legume root nodule. Annu. Rev. Cell Biol. 7, 191-226.
Cao, Y., Halane, M.K., Gassmann, W. and Stacey, G. (2017) The role of plant innate immunity in the legume-rhizobium symbiosis. Annu. Rev. Plant Biol. 68, 535-561.
Charpentier, M. and Oldroyd, G. (2010) How close are we to nitrogen-fixing cereals? Curr. Opin. Plant Biol. 13, 556-564.
Cole, M.A. and Elkan, G.H. (1973) Transmissible resistance to penicillin G, neomycin, and chloramphenicol in Rhizobium japonicum. Antimicrob. Agents Chemother. 4, 248-253.
Colebatch, G., Desbrosses, G., Ott, T., Krusell, L., Montanari, O., Kloska, S., Kopka, J. and Udvardi, M.K. (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39, 487-512.
de Werra, P., Péchy-Tarr, M., Keel, C. and Maurhofer, M. (2009) Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Appl. Environ. Microbiol. 75, 4162-4174.
Denison, R.F. (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156, 567-576.
Desbrosses, G.G., Kopka, J. and Udvardi, M.K. (2005) Lotus japonicus metabolic profiling. Development of gas chromatography-mass spectrometry resources for the study of plant-microbe interactions. Plant Physiol. 137, 1302-1318.
Ding, Y. and Oldroyd, G.E. (2009) Positioning the nodule, the hormone dictum. Plant Signal. Behav. 4, 89-93.
Faizal, A. and Geelen, D. (2013) Saponins and their role in biological processes in plants. Phytochem. Rev. 12, 877-893.
Fujihara, S. and Yamaguchi, M. (1980) Nitrogen fixation and allantoin formation in soybean plants. Agric. Biol. Chem. 44, 2569-2573.
Gaude, N., Tippmann, H., Flemetakis, E., Katinakis, P., Udvardi, M. and Dörmann, P. (2004) The galactolipid digalactosyldiacylglycerol accumulates in the peribacteroid membrane of nitrogen-fixing nodules of soybean and Lotus. J. Biol. Chem. 279, 34624-34630.
Gemperline, E., Jayaraman, D., Maeda, J., Ané, J.-M. and Li, L. (2015) Multifaceted investigation of metabolites during nitrogen fixation in Medicago via high resolution MALDI-MS imaging and ESI-MS. J. Am. Soc. Mass Spectrom. 26, 149-158.
Gillman, J.D., Stacey, M.G., Cui, Y.Y., Berg, H.R. and Stacey, G. (2014) Deletions of the SACPD-C locus elevate seed stearic acid levels but also result in fatty acid and morphological alterations in nitrogen fixing nodules. BMC Plant Biol. 14, 143.
Gourion, B., Berrabah, F., Ratet, P. and Stacey, G. (2015) Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci. 20, 186-194.
Hahn, M., Meyer, L., Studer, D., Regensburger, B. and Hennecke, H. (1984) Insertion and deletion mutations within the nif region of rhizobium-japonicum. Plant Mol. Biol. 3, 159-168.
Hakoyama, T., Niimi, K., Watanabe, H., Tabata, R., Matsubara, J., Sato, S., Nakamura, Y., Tabata, S., Jichun, L. and Matsumoto, T. (2009) Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature, 462, 514-517.
Hakoyama, T., Niimi, K., Yamamoto, T., Isobe, S., Sato, S., Nakamura, Y., Tabata, S., Kumagai, H., Umehara, Y. and Brossuleit, K. (2011) The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol. 53, 225-236.
Halverson, L.J. and Stacey, G. (1986) Effect of lectin on nodulation by wild-type Bradyrhizobium japonicum and a nodulation-defective mutant. Appl. Environ. Microbiol. 51, 753-760.
Harada, K. and Fukusaki, E. (2009) Profiling of primary metabolite by means of capillary electrophoresis-mass spectrometry and its application for plant science. Plant Biotechnol. 26, 47-52.
Haralampidis, K., Trojanowska, M. and Osbourn, A.E. (2002) Biosynthesis of triterpenoid saponins in plants. In History and Trends in Bioprocessing and Biotransformation (Dutta, N.N., Hammar, F., Haralampidis, K., et al. eds). Vol. 75, Berlin, Heidelberg: Springer, pp. 31-49.
Hardy, R. and Havelka, U. (1975) Nitrogen fixation research: a key to world food? Science, 188, 633-643.
Hause, B. and Schaarschmidt, S. (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry, 70, 1589-1599.
Hossain, M.S., Umehara, Y. and Kouchi, H. (2006) A novel Fix symbiotic mutant of Lotus japonicus, Ljsym105, shows impaired development and premature deterioration of nodule infected cells and symbiosomes. Mol. Plant-Microbe Interact. 19, 780-788.
Hostettmann, K. and Marston, A. (2005) Saponins. Cambridge: Cambridge University Press.
Hunter, J.E., Zhang, J. and Kris-Etherton, P.M. (2009) Cardiovascular disease risk of dietary stearic acid compared with trans, other saturated, and unsaturated fatty acids: a systematic review. Am. J. Clin. Nutr. 91, 46-63.
Hunter, W.J. (1983) Soybean root and nodule nitrate reductase. Physiol. Plant. 59, 471-475.
Kachroo, A., Fu, D.-Q., Havens, W., Navarre, D., Kachroo, P. and Ghabrial, S.A. (2008) An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Mol. Plant-Microbe Interact. 21, 564-575.
Kachroo, A., Shanklin, J., Whittle, E., Lapchyk, L., Hildebrand, D. and Kachroo, P. (2007) The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol. Biol. 63, 257-271.
Karr, D., Emerich, D. and Karr, A. (1992) Accumulation of the phytoalexin, glyceollin, in root nodules of soybean formed by effective and ineffective strains of Bradyrhizobium japonicum. J. Chem. Ecol. 18, 997-1008.
Kawaguchi, M., Imaizumi-Anraku, H., Koiwa, H., Niwa, S., Ikuta, A., Syono, K. and Akao, S. (2002) Root, root hair, and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant-Microbe Interact. 15, 17-26.
Kemen, A.C., Honkanen, S., Melton, R.E., Findlay, K.C., Mugford, S.T., Hayashi, K., Haralampidis, K., Rosser, S.J. and Osbourn, A. (2014) Investigation of triterpene synthesis and regulation in oats reveals a role for β-amyrin in determining root epidermal cell patterning. Proc. Natl Acad. Sci. USA, 111, 8679-8684.
Kiers, E.T., Rousseau, R.A., West, S.A. and Denison, R.F. (2003) Host sanctions and the legume-rhizobium mutualism. Nature, 425, 78-81.
Koo, A.J. (2018) Metabolism of the plant hormone jasmonate: a sentinel for tissue damage and master regulator of stress response. Phytochem. Rev. 17, 51-80.
Krishnan, H.B., Alaswad, A.A., Oehrle, N.W. and Gillman, J.D. (2016) Deletion of the SACPD-C locus alters the symbiotic relationship between Bradyrhizobium japonicum USDA110 and soybean, resulting in elicitation of plant defense response and nodulation defects. Mol. Plant-Microbe Interact. 29, 862-877.
Kumagai, H., Hakoyama, T., Umehara, Y., Sato, S., Kaneko, T., Tabata, S. and Kouchi, H. (2007) A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus. Plant Physiol. 143, 1293-1305.
Laith, A.Z., Rikkita, K., Tina, T.H. et al. (2020) Single-cell metabolic profiling: metabolite formulas from isotopic fine structures in heterogeneous plant cell populations. Anal. Chem. 92(10), 7289-7298. https://doi.org/10.1021/acs.analchem.0c00936
Lakhssassi, N., Colantonio, V., Flowers, N.D., Zhou, Z., Henry, J., Liu, S. and Meksem, K. (2017) Stearoyl-acyl carrier protein desaturase mutations uncover an impact of stearic acid in leaf and nodule structure. Plant Physiol. 174, 1531-1543.
Lardi, M., Murset, V., Fischer, H.-M., Mesa, S., Ahrens, C.H., Zamboni, N. and Pessi, G. (2016) Metabolomic profiling of Bradyrhizobium diazoefficiens-induced root nodules reveals both host plant-specific and developmental signatures. Int. J. Mol. Sci. 17, 815.
Larrainzar, E., Wienkoop, S., Weckwerth, W., Ladrera, R., Arrese-Igor, C. and González, E.M. (2007) Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiol. 144, 1495-1507.
LeVier, K., Day, D.A. and Guerinot, M.L. (1996) Iron uptake by symbiosomes from soybean root nodules. Plant Physiol. 111, 893-900.
Li, H., Balan, P. and Vertes, A. (2016) Molecular imaging of growth, metabolism, and antibiotic inhibition in bacterial colonies by laser ablation electrospray ionization mass spectrometry. Angew. Chem. Int. Ed. 55, 15035-15039.
Libault, M. (2018) Transcriptional reprogramming of legume genomes: perspective and challenges associated with single-cell and single cell-type approaches during nodule development. Front. Plant Sci. 9, 1600.
Liechti, R. and Farmer, E.E. (2002) The jasmonate pathway. Science, 296, 1649-1650.
Lim, G.-H., Singhal, R., Kachroo, A. and Kachroo, P. (2017) Fatty acid-and lipid-mediated signaling in plant defense. Annu. Rev. Phytopathol. 55, 505-536.
Loh, J.T., Yuen-Tsai, J.P.Y., Stacey, M.G., Lohar, D., Welborn, A. and Stacey, G. (2001) Population density-dependent regulation of the Bradyrhizobium japonicum nodulation genes. Mol. Microbiol. 42, 37-46.
Maunoury, N., Redondo-Nieto, M., Bourcy, M., Van de Velde, W., Alunni, B., Laporte, P., Durand, P., Agier, N., Marisa, L. and Vaubert, D. (2010) Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. PLoS ONE, 5, e9519.
Mergaert, P., Uchiumi, T., Alunni, B., Evanno, G., Cheron, A., Catrice, O., Mausset, A.-E., Barloy-Hubler, F., Galibert, F. and Kondorosi, A. (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc. Natl Acad. Sci. USA, 103, 5230-5235.
Miwa, H., Sun, J., Oldroyd, G.E. and Allan Downie, J. (2006) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J. 48, 883-894.
Moreau, S., Day, D.A. and Puppo, A. (1998) Ferrous iron is transported across the peribacteroid membrane of soybean nodules. Planta, 207, 83-87.
Moreau, S., Meyer, J.-M. and Puppo, A. (1995) Uptake of iron by symbiosomes and bacteroids from soybean nodules. FEBS Lett. 361, 225-228.
Nakagawa, T. and Kawaguchi, M. (2006) Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol. 47, 176-180.
Nemes, P., Barton, A.A., Li, Y. and Vertes, A. (2008) Ambient molecular imaging and depth profiling of live tissue by infrared laser ablation electrospray ionization mass spectrometry. Anal. Chem. 80, 4575-4582.
Nemes, P. and Vertes, A. (2007) Laser ablation electrospray ionization for atmospheric pressure, in vivo, and imaging mass spectrometry. Anal. Chem. 79, 8098-8106.
Novák, K., Lisá, L. and Škrdleta, V. (2004) Rhizobial nod gene-inducing activity in pea nodulation mutants: dissociation of nodulation and flavonoid response. Physiol. Plant. 120, 546-555.
Oldroyd, G.E. (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252-263.
Oldroyd, G.E. and Downie, J.A. (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546.
Oono, R., Anderson, C.G. and Denison, R.F. (2011) Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proc. Roy. Soc. Lond. B Biol. Sci. 278, 2698-2703.
Parniske, M., Zimmermann, C., Cregan, P. and Werner, D. (1990) Hypersensitive reaction of nodule cells in the glycine sp./Bradyrhizobium japonicum-symbiosis occurs at the genotype-specific level. Botanica Acta, 103, 143-148.
Pauwels, L., Inzé, D. and Goossens, A. (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14, 87-91.
Pislariu, C.I., Sinharoy, S., Torres-Jerez, I., Nakashima, J., Blancaflor, E.B. and Udvardi, M.K. (2019) The nodule-specific PLAT domain protein NPD1 is required for nitrogen-fixing symbiosis. Plant Physiol. 180, 1480-1497.
Prell, J. and Poole, P. (2006) Metabolic changes of rhizobia in legume nodules. Trends Microbiol. 14, 161-168.
Regus, J., Gano, K., Hollowell, A., Sofish, V. and Sachs, J. (2015) Lotus hosts delimit the mutualism-parasitism continuum of B radyrhizobium. J. Evol. Biol. 28, 447-456.
Regus, J.U., Quides, K.W., O'Neill, M.R., Suzuki, R., Savory, E.A., Chang, J.H. and Sachs, J.L. (2017) Cell autonomous sanctions in legumes target ineffective rhizobia in nodules with mixed infections. Am. J. Bot. 104, 1299-1312.
Rosendahl, L., Glenn, A.R. and Dilworth, M.J. (1991) Organic and inorganic inputs into legume root nodule nitrogen fixation. In Biology and biochemistry of nitrogen fixation (Dilworth, M.J., and Glenn, A.R., eds). London: Elsevier London, pp. 259-291.
Roth, L. and Stacey, G. (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur. J. Cell Biol. 49, 13-23.
Sachs, J., Russell, J., Lii, Y., Black, K., Lopez, G. and Patil, A. (2010) Host control over infection and proliferation of a cheater symbiont. J. Evol. Biol. 23, 1919-1927.
Sadowsky, M.J., Cregan, P.B., Gottfert, M., Sharma, A., Gerhold, D., Rodriguez-Quinones, F., Keyser, H.H., Hennecke, H. and Stacey, G. (1991) The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans. Proc. Natl Acad. Sci. USA, 88, 637-641.
Sagan, M., Morandi, D., Tarenghi, E. and Duc, G. (1995) Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after γ-ray mutagenesis. Plant Sci. 111, 63-71.
Sanchez, F., Padilla, J.E., Perez, H. and Lara, M. (1991) Control of nodulin genes in root-nodule development and metabolism. Annu. Rev. Plant Biol. 42, 507-528.
Sandal, N., Petersen, T.R., Murray, J., Umehara, Y., Karas, B., Yano, K., Kumagai, H., Yoshikawa, M., Saito, K. and Hayashi, M. (2006) Genetics of symbiosis in Lotus japonicus: recombinant inbred lines, comparative genetic maps, and map position of 35 symbiotic loci. Mol. Plant-Microbe Interact. 19, 80-91.
Sanjuan, J., Grob, P., Goettfert, M., Hennecke, H. and Stacey, G. (1994) NodW is essential for full expression of the common nodulation genes in Bradyrhizobium japonicum. Mol. Plant Microbe Interact. 7, 364-369.
Sato, T., Yashima, H., Ohtake, N., Sueyoshi, K., Akao, S., Harper, J.E. and Ohyama, T. (1998) Determination of leghemoglobin components and xylem sap composition by capillary electrophoresis in hypernodulation soybean mutants cultivated in the field. Soil Sci. Plant Nutr. 44, 635-645.
Shanklin, J. and Cahoon, E.B. (1998) Desaturation and related modifications of fatty acids. Annu. Rev. Plant Biol. 49, 611-641.
Simms, E.L., Taylor, D.L., Povich, J., Shefferson, R.P., Sachs, J., Urbina, M. and Tausczik, Y. (2005) An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proc. Roy. Soc. B Biol. Sci. 273, 77-81.
Singleton, P. and Stockinger, K. (1983) Compensation against ineffective nodulation in soybean 1. Crop Sci. 23, 69-72.
Smith, P.M. and Atkins, C.A. (2002) Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiol. 128, 793-802.
Soedarjo, M. and Borthakur, D. (1998) Mimosine, a toxin produced by the tree-legume Leucaena provides a nodulation competition advantage to mimosine-degrading Rhizobium strains. Soil Biol. Biochem. 30, 1605-1613.
Soga, T., Ohashi, Y., Ueno, Y., Naraoka, H., Tomita, M. and Nishioka, T. (2003) Quantitative metabolome analysis using capillary electrophoresis mass spectrometry. J. Proteome Res. 2, 488-494.
Spaink, H.P., Sheeley, D.M., van Brussel, A.A., Glushka, J., York, W.S., Tak, T., Geiger, O., Kennedy, E.P., Reinhold, V.N. and Lugtenberg, B.J. (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature, 354, 125.
Spaink, H.P., Wijffelman, C.A., Pees, E., Okker, R.J. and Lugtenberg, B. (1987) Rhizobium nodulation gene nodD as a determinant of host specificity. Nature, 328, 337.
Stacey, G. (2007) The Rhizobium-legume nitrogen-fixing symbiosis. In Biology of the Nitrogen Cycle (Bothe, H., Ferguson, S.J., and Newton, W.E., eds). London: Elsevier, p. 147-163.
Stacey, G., Libault, M., Brechenmacher, L., Wan, J. and May, G.D. (2006) Genetics and functional genomics of legume nodulation. Curr. Opin. Plant Biol. 9, 110-121.
Stopka, S.A., Agtuca, B.J., Koppenaal, D.W., Paša-Tolić, L., Stacey, G., Vertes, A. and Anderton, C.R. (2017) Laser ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia. Plant J. 91, 340-354.
Stopka, S.A., Khattar, R., Agtuca, B.J., Anderton, C.R., Paša-Tolić, L., Stacey, G. and Vertes, A. (2018) Metabolic noise and distinct subpopulations observed by single cell LAESI mass spectrometry of plant cells in situ. Front. Plant Sci. 9, 1646.
Stopka, S.A., Samarah, L.Z., Shaw, J.B. et al. (2019) Ambient metabolic profiling and imaging of biological samples with ultrahigh molecular resolution using laser ablation electrospray ionization 21 Tesla FTICR mass spectrometry. Anal. Chem. 91(8), 5028-5035. https://doi.org/10.1021/acs.analchem.8b05084
Suganuma, N., Nakamura, Y., Yamamoto, M., Ohta, T., Koiwa, H., Akao, S. and Kawaguchi, M. (2003) The Lotus japonicus Sen1 gene controls rhizobial differentiation into nitrogen-fixing bacteroids in nodules. Mol. Genet. Genomics, 269, 312-320.
Sun, J., Cardoza, V., Mitchell, D.M., Bright, L., Oldroyd, G. and Harris, J.M. (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J. 46, 961-970.
Tóth, K. and Stacey, G. (2015) Does plant immunity play a critical role during initiation of the legume-rhizobium symbiosis? Front. Plant Sci. 6, 401.
Tsuno, Y., Fujimatsu, T., Endo, K., Sugiyama, A. and Yazaki, K. (2017) Soyasaponins, a new class of root exudates in soybean (Glycine max). Plant Cell Physiol. 59, 366-375.
Udvardi, M. and Poole, P.S. (2013) Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol. 64, 781-805.
Vance, C. and Heichel, G. (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu. Rev. Plant Biol. 42, 373-390.
Veereshlingam, H., Haynes, J.G., Penmetsa, R.V., Cook, D.R., Sherrier, D.J. and Dickstein, R. (2004) nip, a symbiotic Medicago truncatula mutant that forms root nodules with aberrant infection threads and plant defense-like response. Plant Physiol. 136, 3692-3702.
Veličković, D., Agtuca, B.J., Stopka, S.A., Vertes, A., Koppenaal, D.W., Paša-Tolić, L., Stacey, G. and Anderton, C.R. (2018) Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange. ISME J. 12, 2335-2338.
Vicente, E.J. and Dean, D.R. (2017) Keeping the nitrogen-fixation dream alive. Proc. Natl Acad. Sci. USA, 114, 3009-3011.
Wang, J.Y., Si, Z.Y., Li, F., Xiong, X.B., Lei, L., Xie, F.L., Chen, D.S., Li, Y.X. and Li, Y.G. (2015) A purple acid phosphatase plays a role in nodule formation and nitrogen fixation in Astragalus sinicus. Plant Mol. Biol. 88, 515-529.
Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100, 681-697.
Wasternack, C. and Hause, B. (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021-1058.
Yamaya-Ito, H., Shimoda, Y., Hakoyama, T., Sato, S., Kaneko, T., Hossain, M.S., Shibata, S., Kawaguchi, M., Hayashi, M. and Kouchi, H. (2017) Loss-of-function of ASPARTIC PEPTIDASE NODULE-INDUCED 1 (APN1) in Lotus japonicus restricts efficient nitrogen-fixing symbiosis with specific Mesorhizobium loti strains. Plant J. 93, 5-16.
Ye, H., Gemperline, E., Venkateshwaran, M., Chen, R., Delaux, P.M., Howes-Podoll, M., Ané, J.M. and Li, L. (2013) MALDI mass spectrometry-assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula-Sinorhizobium meliloti symbiosis. Plant J. 75, 130-145.
Zdyb, A., Demchenko, K., Heumann, J., Mrosk, C., Grzeganek, P., Göbel, C., Feussner, I., Pawlowski, K. and Hause, B. (2011) Jasmonate biosynthesis in legume and actinorhizal nodules. New Phytol. 189, 568-579.
Zhang, N., Venkateshwaran, M., Boersma, M., Harms, A., Howes-Podoll, M., den Os, D., Ané, J.-M. and Sussman, M.R. (2012) Metabolomic profiling reveals suppression of oxylipin biosynthesis during the early stages of legume-rhizobia symbiosis. FEBS Lett. 586, 3150-3158.

Auteurs

Beverly J Agtuca (BJ)

Divisions of Plant Sciences and Biochemistry, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.

Sylwia A Stopka (SA)

Department of Chemistry, The George Washington University, Washington, DC, 20052, USA.

Sterling Evans (S)

Divisions of Plant Sciences and Biochemistry, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.

Laith Samarah (L)

Department of Chemistry, The George Washington University, Washington, DC, 20052, USA.

Yang Liu (Y)

Department of Electrical Engineering and Computer Science, Informatics Institute and Christopher S. Bond Life Sciences Center, University of Missouri-Columbia, Columbia, MO, 65211, USA.

Dong Xu (D)

Department of Electrical Engineering and Computer Science, Informatics Institute and Christopher S. Bond Life Sciences Center, University of Missouri-Columbia, Columbia, MO, 65211, USA.

Minviluz G Stacey (MG)

Divisions of Plant Sciences and Biochemistry, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.

David W Koppenaal (DW)

Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, 902 Battelle Boulevard, Richland, WA, 99354, USA.

Ljiljana Paša-Tolić (L)

Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, 902 Battelle Boulevard, Richland, WA, 99354, USA.

Christopher R Anderton (CR)

Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, 902 Battelle Boulevard, Richland, WA, 99354, USA.

Akos Vertes (A)

Department of Chemistry, The George Washington University, Washington, DC, 20052, USA.

Gary Stacey (G)

Divisions of Plant Sciences and Biochemistry, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.

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